Research on Anolis lizards and other notes on evolutionary biology, herpetology and life as a scientist

As an educator at the American Museum of Natural History, I knew enough about paleontology to tell people that there were no known aquatic dinosaurs. To many peoples’ surprise plesiosaurs, icthyosaurs, mosasaurs (and all the other fossil marine reptiles so often depicted in books and TV shows) – none of them were actually dinosaurs. They were very different types of reptiles, extinct sauropterygians and icthyopterygians (mosasaurs were actually a kind of lizard) that lived in the seas during the Mesozoic Era while dinosaurs ruled the land.

Jurassic Park 3 came out in 2001, which featured a Spinosaurus that swam like a crocodile, and all the people were like, “See! Dinosaurs COULD swim!” But I never said dinosaurs couldn’t swim. There has long been fossil evidence – in the form of trackways that resemble scraped claws against river floors – that dinosaurs probably were pretty good swimmers, and waterways wouldn’t have presented much of a dispersal barrier, just like caribou and other large modern migrating animals who eventually encounter water at some point in their life and have to cross it. Still, there were no fossil remains ever described as belonging to a dinosaur that actually lived in the water.

Since it’s discovery over 100 years ago, Spinosaurus has been known as one of the largest theropods. Theropods are a large group of dinosaurs which includes not only all birds but all the familiar carnivorous species, including Allosaurus and Velociraptor. Spinosaurus was bigger than even the biggest Tyrannosaurus. This week, the journal Science published the paper “Semiaquatic Adaptations in a Giant Predatory Dinosaur“, in which a group of scientists make the case for a long list of adaptations supporting the idea that this huge meat-eating dinosaur with a sail on its back was also well adapted to life in the water.

Finally, a dinosaur that lived in the water and swam and ate fish like a crocodile. I have been waiting my whole life for there to be one, and here it was under our noses the whole time. Good ol’ Spinosaurus. Museum educators will have to adjust their curriculum accordingly.

This is the second post in my series on my favorite examples of convergent evolution, a concept which I defined previously and demonstrated with marsupial and placental wolves. That post featured two modern terrestrial mammalian species with relatively recent evolutionary histories. For the current example, I would like to take us into the oceans and examine a much wider range of organisms as disparate as cartilaginous fish, bony fish, reptiles and mammals — spanning about 530,000,000 years of Earth’s history. Within each of these highly divergent lineages, a particular adaptation for high-speed underwater movement evolved, known as thunniform locomotion – which means literally “swimming like a tuna”.

The thunniform body plan consists of a suite of traits that makes an animal a streamlined swimming apparatus: a rigid anterior section (from the head to about the pelvic region) that becomes much more flexible posteriorly, with a crescent-shaped caudal fin (a.k.a tail fin or fluke). A thunniform swimmer need only to undulate its caudal region (meaning basically its tail) and the result is efficient propulsion through the watery medium with minimal head-wiggling (see Figure1). Thus, the swimmer can disperse over long oceanic distances at high speeds, and keep its eyes toward whatever its pursuing. That this has evolved in so many different types of top marine predators over the eons strongly suggests that the common environment of the ocean presents strong selective pressure for an optimal form of locomotion. In sharks and tuna, thunniform locomotion represents more of a parallel pattern of evolution, which is is when two separate lineages evolve into similar forms independently but had mostly similar starting points (the common ancestor of sharks and tuna was already aquatic). It is even more remarkable, in my opinion, that it developed in both reptiles and mammals, since the common ancestor of these groups lived on land. The convergent evolution of this highly derived body shape thus required totally independent exoduses of terrestrial animals back into the ocean.

Among the many kinds of reptiles that inhabited the world’s oceans during the Mesozoic Era, there were none so well-suited to marine life as the ichthyosaurs (“fish lizards”). The ichthyosaurs are the most highly derived group within the reptilian superorder Ichthyopterygia, which were ocean-going reptiles who had developed their characteristic “fish flippers” very early on in their history. It is generally accepted that the ancestors of the ichthyopterygians were land-dwelling amniotes, however the precise taxonomy of their relationships to other reptiles has been highly contentious and was hotly debated throughout the 20th century. This is because the fossil record is devoid of any transitional forms that could be seen as terrestrial precursors – the oldest ichthyopterygian fossils, which date to the Early Triassic ~250,000,000 years ago, are already so “ichthyosaurian” – and it is extremely difficult to retrace the evolutionary steps taken towards their aquatic lifestyle. However, most modern cladistic analyses indicate that ichthyopterygians were diapsid reptiles along with lepiodsaurs (snakes, lizards and tuatara) and archosaurs (crocodilians, pterosaurs, and avian and non-avian dinosaurs) (Motani et al. 1998).

Soon after reptiles started dominating terrestrial environments during the early Mesozoic, they began to conquer the sea as well. But by about 90,000,000 years ago, the last ichthyosaurs died out. Regardless of their ancestry and the length of time they have been extinct, the ichthyosaurs just might represent my favorite historical example of convergent evolution. Figure 2 shows a skeletal and a life restoration of the iconic Ichthyosaurus communis and demonstrates just how well-adapted these animals were to marine life. The overall shape of the body is reminiscent of a streamlined torpedo. The hands and fingers on its front limbs became pectoral fins; other fins included a dorsal fin that is more obvious in fossil impressions as well as a crecsent-shaped caudal fin that makes the tail look very shark-like. You can see how lateral (side-to-side) undulation of its rear end would thrust the animal forward through the water with minimal effort. I included a dolphin skeleton in the figure to highlight how precise the convergence between these two highly divergent vertebrates was. They do undulate on different axes; dolphins thrust their tails up-and-down, not side-to-side, but that seems to be a strongly conserved trait among mammalian swimmers and I think it doesn’t take away from the overall similarities. The evolution of whales and dolphins from their terrestrial ancestors that began ~55 million years ago is another amazing evolutionary story that I won’t get into here. What I wanted to highlight in this post is how closely these air-breathing vertebrates came to resemble one another.

A very good overview of the various forms of undulatory locomotion, including thunniform, can be found here.

Figure 1. Different and divergent species are each adapted to their unique environments (in this case, camouflage) are represented as polygons against a different color background. Environmental change causes each separate habitat to become more similar, and in response to this change, over time each species independently evolves similar adaptations (in this case, green camouflage).

One of my favorite evolutionary phenomena to talk (and write) about is convergent evolution. Convergence has occurred whenever phylogenetically distant species, in either or both disparate geographic regions or geological epochs, have evolved very similar phenotypes. This is usually due to similar ecological conditions across the times and places in which the species reside, and in response to similar selective pressures, the different species have in common parallel yet independently evolved adaptations (this concept is illustrated in Figure 1). These similarities are not due to common ancestry and are therefore not homologous. It seems that this would be rare pattern, however the tree of life is full of amazing examples of convergence, and the prevalence of convergence throughout Earth’s history suggests there is at least some degree of determinism in the evolutionary process. I want to write a series of posts which highlight some of my favorite examples of convergent evolution. These posts will try to frame each case in evolutionary, biogeographical, anatomical, and environmental terms.

Figure 2. Lobo (the King of Currumpaw), by Ernest Thompson Seton, one of my favorite wolves. Image in the Public Domain.

My first case study in convergent evolution will be the wonderful story of two predatory mammals, which lived at approximately the same time but in separate corners of the globe. One of these is extinct and the other… well it’s complicated. During the Miocene Era which lasted between ~23,000,000 and ~5,200,000 years ago, an environmental change occurred which allowed vast grasslands to open across Eurasia, and with that, the development of a diverse community of crown-toothed herbivorous perissodactyls (“odd-toed” ungulates which include modern-day horses and rhinos) and artiodactyls (“even-toed” ungulates which include modern day cows, sheep and camels) which grazed and browsed across the new prairies. Not surprisingly, there were carnivores which became adapted to chasing down this quick quarry, including canids (the dog family, which includes foxes, jackals and wolves). Most folks are familiar with wolves. Modern wolves (Canis lupus) likely appeared during the early to middle Pleistocene (between ~2,500,000 and 1,000,000 years ago), and are slender, powerful predators adapted to pursuing similarly-sized prey over long distances. They have deep chests and long legs, reminiscent of distance runners, and bone-crunching jaws with pointy canines well-suited for holding onto prey (say, for instance, a fleeing deer), as well as scissor-like carnassial teeth for meat-slicing. No wonder wolves have inhabited a special place in the human psyche – with results that were often bad for wolves. I love wolves, and as a teenager I was mesmerized by reading about their natural history as well as accounts of human-wolf interactions (which often bordered on the fictional), such as “Lobo the King of Currumpaw” by Ernest Thompson Seton in Wild Animals I HaveKnown (1898) (Figure 2),and especially that of “Thinking Like a Mountain” by Aldo Leopold in A Sand County Almanac (1949), where Leopold recalls the moment he changed from wolf-hater/hunter to one of the pioneers of the environmental and conservation movements. If you ask me, a better appeal for whole-ecosystem conservation has never been written:

We reached the old wolf in time to watch a fierce green fire dying in her eyes. I realized then, and have known ever since, that there was something new to me in those eyes – something known only to her and to the mountain. I was young then, and full of trigger-itch; I thought that because fewer wolves meant more deer, that no wolves would mean hunters’ paradise. But after seeing the green fire die, I sensed that neither the wolf nor the mountain agreed with such a view.

Let’s turn back the clock and take a trip to the the land down under, where after the breakup of the supercontinent Gondwana during the Jurassic Period ~200,000,000 years ago, the resident life forms were stranded at sea on an island landmass known as Australia. Placental mammals had not yet dispersed globally, and the only members of the furred kind in Australia at the time of the continental breakup were the pouched marsupials – and it remained that way until very recently (when humans brought their rats and sheep). During the Miocene, as in Eurasia, grasslands began to open up across Australia, although many regions were still heavily forested. This created many new and unique niches that allowed the resident marsupials to adapt and radiate into a wide variety of forms, such as diprotodonts (which include arboreal possums, familiar and bounding kangaroos, and the extinct large lumbering herbivore Diporotodon), and dasyurids which include the Tasmanian devil and Tasmanian wolf (Figure 3). Wolf? Yes, there is a marsupial wolf. How can that be? The answer is: CONVERGENCE. The scientific name of the Tasmanian wolf is Thylacinus cynocephalus, which means “pouched animal with the head of a dog”. Another more unique and accurate common name is the thylacine.

Thylacines appeared in Australia during the Miocene, and the modern species was present in both Australia and Tasmania by the Pleistocene and into the Holocene, although it was just about absent from mainland Australia by the 1800s and restricted to Tasmania by the 20th century. Just as wolves across Eurasia and North America, thylacines were looked upon as threats to ranchers and were accused of killing chickens and sheep. As a result, they were hunted to extinction and the last one died in a zoo in the Hobart Zoo in Tasmania in 1938. The thylacine was a dog-sized predator, and while its method of prey acquisition is still under debate (whether it was a pursuit predator like wolves or more of an ambush predator like a cougar), together with canids it represents an exceptional case of convergent evolution, which is most evident in a comparison of the cranial anatomy with C. lupus (Figure 4). Both species have an elongated snout with pointed canines and scissor-like molars which are well suited for snapping up, killing and dismembering prey. You’d be hard-pressed to pick one or the other out of a line-up. One of the few cranial traits that can be used as a clue is that the thylacine has more teeth overall, including triangular-shaped molars, thus betraying its marsupial ancestry. But you’d have to be an expert to notice that. While they lived on opposite ends of the world, placental canids and marsupial thylacines developed into similar ecological roles and responded with a convergent evolution toward extremely similar phenotypes.

As mentioned above, while thylacines and wolves evolved into similar forms, they also were met with similar antagonism by humans. Alas, the thylacine died out before the conservation movement took hold. With their much wider distribution across the Northern Hemisphere, placental wolves were able to hold in many areas and were more recently aided by human efforts to bolster their recovery. As Aldo Leopold predicted, the reintroduction of wolves into Yellowstone National Park was a major triumph for conservation, as it returned a keystone species to an ecosystem which was out of equilibrium due to its absence. The return of the thylacine would require either a seance or de-extinctioning through DNA cloning. The probabilities of either of those producing a living thylacine anytime soon are close to zero.

It’s a good week for snake genomics, because PNAS has published both the Burmese python genome (Castoe et al. 2013) and the king cobra genome (Vonk et al. 2013). The related papers come from separate research teams (the python people mostly from Colorado and the cobra cabal the Netherlands), albeit with significant overlap between them. The world of snake molecular biology is a small one, after all.

Figure 3B from Castoe et al. (2013), showing genes that have undergone positive selection on the vertebrate lineage leading to snakes.

The authors of the python paper also investigated how snakes evolved their iconic and constrained morphology – because, after all, snakes lack legs and are equipped with a feeding apparatus equivalent to a human being swallowing a 16lb Thanksgiving turkey whole, and the molecular bases of these adaptations are unresolved. They analyzed a large number of genes shared across vertebrates – called orthologs – and found that during the evolution of the vertebrate lineage leading to snakes, many genes associated with skull and spinal development, metabolism and other functions experienced a faster rate of evolution than in other lineages. Also very cool.

Next up: king cobra. Why do we need both a python AND a cobra genome? The answer lies in the difference between these two snakes. One of them – and I hope you guessed cobra – is venomous. So it is no surprise that much of the justification for sequencing the king cobra genome included a need to understand the evolutionary origins and maintenance of the genes that control venom production. The cobra genome contains a multitude of protein families that underwent a significant expansion during cobra evolution that resulted in what we see today – a highly potent mixture of toxins designed to ensure certain death to a chosen prey item.

The two genomes differ vastly in their qualities of assembly. Through a mixture of various sequencing methods, the python team was able to get an N50 value of 207kb, meaning 50% of the assembled chunks of contiguous sequence were at least 207,000 base pairs of DNA in length. That assures that the research team would be able to recover the majority of genes – exons and introns and all. The cobra genome by contrast has an N50 value of only 3,982 base pairs, meaning that some of the genes may be fragmentary and the length of many introns will remain unresolved. However, I think that using N50 as a the gold standard of genome assembly “quality” is misleading. Sequencing strategies that significantly raise N50 values cost more money. In this day and age of modern biology, where small labs or groups of researchers conjure up whatever resources they can for an in-house genome sequencing project, the most affordable strategy for however you wish to address your biological questions will probably suffice. Both of these snake genome papers make the cut in that regard, and they are a significant contribution to the field of reptilian genomics.

Earlier in the year, I graduated, was removed from the pressure of a dissertation and hired by another lab, based on merit, to dedicate my days solely to conducting research in the burgeoning field of genomics. Reptilian genomics, at that. It’s a dream job! Very few early-career scholars in biology can lay claim to being literally handed the job they always wanted. A postdoc, while not exactly raining in the Benjamins like some high-priced lawyer or marketing exec, is a proud position to have – a GENIUS FOR HIRE. Right?

Well, it is great. But not all roses. Even though my current appointment is long by most standards, almost by definition it’s a temporary position. An “in-betweener” state. By golly, I’ll make the most of the resources given to me here (I aways have – I’m a practical man), but there is the stark reality that I am not that far from “I need a job” – a professorship, what grown-ups in my field have. The tenure-track faculty position will be elusive quarry for even my most competitive peers, and even though I just started my postdoc, every day in the back of my mind lay the specter of the fact that I need to plan for the day I face a search committee. All well and good, I knew what I was getting into, but then there is the weekly perusing of the progress of other postdoctoral scholars in my field, those who got their Ph.Ds in the last two years or so like me, but have slightly better academic pedigrees, or maybe nailed good fellowships, or got published in the REALLY good journals… Oooooh, when envy kicks in, it’s a bad feeling. How will I provide for my family? Also, how can I reconcile these uncertainties with my spouse’s own career ambitions? What to do?

Parent stuff.

We have a 2.5 year old daughter, who we love with all our hearts and is a pure gift. When I’m with her, I find myself concentrating on the real, true things in life, such as fairness, equality, lovingness, and patience. She is the best learner I know, and getting wiser everyday. She is a musician, naturalist, an artist. And a chatter-box, mama mia! She makes every day a joyous journey. Right?

Well, yes and no. Toddler-hood is a messy state of affairs. Zero to sixty in ten seconds with emotions. Tear-the-house-down kind of tantrums. Total lack of ability to follow instructions or obey warnings. Trouble staying in bed in order to fall asleep, and then actually staying in bed all night is another story all together. And then there’s the kid (ba-bum ching). But seriously, the way I have described the feeling of parenthood to others is this: imagine you are a muscle, and you’re always being flexed and flexed, no relaxing. Just one long, never-ending onslaught of work, an eternal set at the gym. And that’s it, that’s what it is, so imagine that if you can (plus a lot of good parts). What to do?

You need to relax.

At this point, I am who I am. Any shortcomings of mine as far as being a scientist or a parent are part of the same continuum. I’m still early in my career post-grad school and post-daughter-being-born. But my postdoc won’t last forever, and neither will toddler-hood. And as time goes by, I’ll get the hang of things. I’ll get a fellowship or a grant and a big paper, because I’m good at a lot of things, and I’ll keep on. We are both talented and savvy, and I’ll find a job that fits the life that we want to have. And our daughter will grow out of her current developmental phase, and with our loving care and guidance, eventually grow into a teenager.

Last weekend I took a night trip out with the Suizo Project. The project’s hard working leaders use radio telemetry to record the movements and key life history traits of rattlesnakes living in the Suizo Mountains in Pinal County, Arizona, which is in the heart of the Sonoran Desert. You can view their Facebook page for project updates here. This was beautiful country and the time of year couldn’t be more perfect: the hot and humid monsoon which plagues the region every summer has officially ended (and so have the days which reach 100 degrees Fahrenheit by 10am and 108 by 3pm). While it still gets hot in the Valley of the Sun near Phoenix (100+, occasionally but not for long), down south in the mountainous Suizo area closer to Tucson (close to 3000 feet at the site I was told) it is simply lovely. The moon was a few days after full, and through the clear and dry desert sky the landscape glowed in a cool blue nightlight. Throughout the evening the temperatures stayed in the 70s and it was the type of night you spend on top of, but not inside, your sleeping bag.

After sundown we embarked on a five hour trek, meaning I followed the knowledgable and experienced guys around the desert and completely took advantage of their skill and expertise in order to learn a lot of things and take a few pictures (I’m not ashamed). Let me just say that in academia, I meet a lot of folks who know a lot about a lot of things but these. Guys. Know. Rattlesnakes. They are experts who can school anyone in the natural history of these incredibly fascinating species – the seasonality of their movements, their food preferences, their mating strategies, their evolution and the environment in which they live.

Some gratuitous musing:

Throughout the 20th century and into today, biology has evolved into ever more specific sub-disciplines, each noble in their own right yet many increasingly cordoned into a sterile laboratory or anonymous computer server, removed from the true natural world. I think the subject of natural history still has its place as a philosophy, a method and appreciation of understanding how the world works. It was after all what inspired me to become an evolutionary biologist.

A female tiger rattlesnake (Crotalus tigris). Note the cactus spines lodged into the scales on her face and torso (yes, snakes have a torso, there’s more to them than a head and a tail). Despite these difficulties, she was in a rather accommodating mood.

Nice shot of the same tiger rattler from above, to highlight its beautiful markings

Western Diamond-backed Rattlesnake (Crotalus atrox). I crossed the continent hoping to see these guys in their natural habitat, and I was ecstatic to see this one. While beautiful and wary of humans, it is extremely venomous (even more so than the other rattlers).

UPDATE [9/27/2013]: I received a response from Marty of the Suizo Project team, who corrected my summation of the relative potencies of rattlesnake venom:

…”extremely venomous, (even more so than other rattlers)” wouldn’t be how I’d describe their venom. They are more venomous, which can be measured in toxicity or volume, than many species of rattlesnakes in terms of volume but few when using LD50 values as a proxy of toxicity. Tiger rattlesnakes, on the other hand, have the most toxic rattlesnake venom but have a small venom yield. Tigers don’t bite people due to their habits and habitat, and relatively small geographic range, while diamondbacks have a comparatively large geographic range, often in close association with people, and are responsible for more human deaths in the U.S. than any other rattlesnake species. It could be said diamondbacks are ‘more deadly’ than other U.S. rattlesnakes…not as in ‘deadly’ in a comparison of toxicity but literally are more deadly because they bite and kill more people – the true measure of deadly!

Thanks for the important distinction, Marty. I wouldn’t want to give diamondbacks a bad name, although we must admit that sadly it is a lost cause…

Marc Tollis

Ph.D. in Ecology, Evolutionary Biology and Behavior program from the City University of New York. Research in population genetics, molecular evolution and comparative genomics. Former music major. Married with child. From Queens and Brooklyn, lives in Tempe, AZ.